SOUL in mouse eyes is a new hexameric heme-binding protein with characteristic optical absorption, resonance raman spectral, and heme-binding properties

Biochemistry

Volumn 43, Issue 44, 2004, Pages 14189-14198

  Sato, Emiko ^a   Sagami, Ikuko ^a,c   Uchida, Takeshi ^b   Sato, Akira ^b   Kitagawa, Teizo ^b   Igarashi, Jotaro ^a   Shimizu, Toni ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b NATIONAL INSTITUTES OF NATURAL SCIENCES   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERS; ESCHERICHIA COLI; HYDROPHOBICITY; LIGHT ABSORPTION; PURIFICATION; TISSUE;

HEME-BONDING PROTEINS; HOMOLOGY; RETINA;

PROTEINS;

BOVINE SERUM ALBUMIN; DIMER; FERRIC ION; FERROUS ION; HEME; HEMOPROTEIN; IRON COMPLEX; LIGAND; MONOMER; PROTEIN P22HBP; PROTEIN SOUL; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; DISSOCIATION CONSTANT; ESCHERICHIA COLI; EYE; GENE EXPRESSION SYSTEM; HYDROPHOBICITY; MOUSE; MUTAGENESIS; NONHUMAN; PINEAL BODY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; RETINA; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CIRCULAR DICHROISM; CLONING, MOLECULAR; EYE PROTEINS; HEME; HEMEPROTEINS; HEMIN; HISTIDINE; LIGANDS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROPHOTOMETRY; SPECTRUM ANALYSIS, RAMAN;

ANIMALIA; BOVINAE; ESCHERICHIA COLI;

EID: 8344236821     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048742i     Document Type: Article

References (55)

1. Antonini, E., and Brunori, M. (1971) Hemoglobin and Myoglobin in Their Reactions with Ligands, Elsevier/North-Holland Biomedical Press, Amsterdam.
2. Poulos, T. (1988) Heme enzyme crystal structures, Adv. Inorg. Biochem. 7, 1-36.
3. Sono, M., Roach, M. P., Coulter, E. D., and Dawson, J. H. (1996) Heme-containing oxygenases, Chem. Rev. 96, 2841-2888.
4. Rodgers, K. R. (1999) Heme-based sensors in biological systems, Curr. Opin. Chem. Biol. 3, 158-167.
5. Gilles-Gonzalez, M. A. (2001) Oxygen signal transduction, IUBMB Life 51, 165-173.
6. Jain, R., and Chan, M. K. (2003) Mechanisms of ligand discrimination by heme proteins, J. Biol. Inorg. Chem. 8, 1-11.
7. Dunham, C. M., Dioum, E. M., Tuckerman, J. R., Gonzalez, G., Scott, W. G., and Gilles-Gonzalez, M. A. (2003) A distal arginine in oxygen-sensing heme-PAS domains is essential to ligand binding, signal transduction, and structure, Biochemistry 42, 7701-7708.
8. Nakamura, H., Kumita, H., Imai, K., Iizuka, T., and Shiro, Y. (2004) ADP reduces the oxygen-binding affinity of a sensory histidine kinase, FixL: the possibility of an enhanced reciprocating kinase reaction, Proc. Natl. Acad. Sci. U.S.A. 101, 2742-2746.
9. Schmidt, P. M., Schramm, M., Schröder, H., Wunder, F., and Stasch, J. P. (2004) Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase, J. Biol. Chem. 279, 3025-3032.
10. Martin, E., Sharina, I., Kots, A., and Murad, F. (2003) A constitutively activated mutant of human soluble guanylyl cyclase (sGC): implication for the mechanism of sGC activation, Proc. Natl. Acad. Sci. U.S.A. 100, 9208-9213.
11. Delgado-Nixon, V. M., Gonzalez, G., and Gilles-Gonzalez, M. A. (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor, Biochemistry 39, 2685-2691.
12. Kurokawa, H., Lee, D. S., Watanabe, M., Sagami, I., Mikami, B., Raman, C. S., and Shimizu, T. (2004) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor, J. Biol. Chem. 279, 20186-20193.
13. Freitas, T. A., Hou, S., and Alam, M. (2003) The diversity of globin-coupled sensors, FEBS Lett. 552, 99-104.
14. Zhan, W., and Phillips, G. N., Jr. (2003) Structure of the oxygen sensor in Bacillus subtilis: signal transduction of chemotaxis by control of symmetry, Structure 11, 1097-1110.
15. Aono, S., Kato, T., Matsuki, M., Nakajima, H., Ohta, T., Uchida, T., and Kitagawa, T. (2002) Resonance Raman and ligand binding studies of the oxygen-sensing signal transducer protein HemAT from Bacillus subtilis, J. Biol. Chem. 277, 13528-13538.
16. Youn, H., Kerby, R. L., and Roberts, G. P. (2003) The role of the hydrophobic distal heme pocket of CooA in ligand sensing and response, J. Biol. Chem. 278, 2333-2340.
17. Aono, S. (2003) Biochemical and biophysical properties of the CO-sensing transcriptional activator CooA, Acc. Chem. Res. 36, 825-831.
18. Dioum, E. M., Rutter, J., Tuckerman, J. R., Gonzalez, G., Gillez-Gonzalez, M. A., and McKnight, S. L. (2002) NPAS2: a gas-responsive transcription factor, Science 298, 2385-2387.
19. Sun, J., Brand, M., Zenke, Y., Tashiro, S., Groudine, M., and Igarashi, K. (2004) Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network, Proc. Natl. Acad. Sci. U.S.A. 101, 1461-1466.
20. Rafie-Kolpin, M., Han, A. P., and Chen, J. J. (2003) Autophosphorylation of threonine 485 in the activation loop is essential for attaining eIF2alpha kinase activity of HRI, Biochemistry 42, 6536-6544.
21. Inuzuka, T., Yun, B. G., Ishikawa, H., Takahashi, S., Hori, H., Matta, R. L., Ishimori, K., and Morishima, I. (2004) Identification of crucial histidines for heme binding in the N-terminal domain of the heme-regulated eIF2alpha kinase, J. Biol. Chem. 279, 6778-6782.
22. Igarashi, J., Sato, A., Kitagawa, T., Yoshimura, T., Yamauchi, S., Sagami, I., and Shimizu, T. (2004) Activation of heme-regulated eukaryotic initiation factor 2alpha kinase by nitric oxide is induced by the formation of a five-coordinate NO-heme complex: optical absorption, electron spin resonance, and resonance Raman spectral studies, J. Biol. Chem. 279, 15752-15762.
23. Zylka, M. J., and Reppert, S. M. (1999) Discovery of a putative heme-binding protein family (SOUL/HBP) by two-tissue suppression subtractive hybridization and database searches, Brain Res. Mol. Brain Res. 74, 175-181.
24. Taketani, S., Adachi, Y., Kohno, H., Ikehara, S., Tokunaga, R., and Ishii, T. (1998) Molecular characterization of a newly identified heme-binding protein induced during differentiation of urine erythroleukemia cells, J. Biol. Chem. 273, 31388-31394.
25. Hargrove, M. S., Barrick, D., and Olson, J. S. (1996) The association rate constant for heme binding to globin is independent of protein structure, Biochemistry 35, 11293-11299.
26. Klatt, P., Schmidt, K., Werner, E. R., and Mayer, B. (1996) Determination of nitric oxide synthase cofactors: heme, FAD, FMN, and tetrahydrobiopterin, Methods Enzymol. 268, 358-365.
27. Sasakura, Y., Hirata, S., Sugiyama, S., Suzuki, S., Taguchi, S., Watanabe, M., Matsui, T., Sagami, I., and Shimizu, T. (2002) Characterization of a direct oxygen sensor heme protein from Escherichia coli. Effects of the heme redox states and mutations at the heme-binding site on catalysis and structure, J. Biol. Chem. 277, 23821-23827.
28. Hirata, S., Matsui, T., Sasakura, Y., Sugiyama, S., Yoshimura, T., Sagami, I., and Shimizu, T. (2003) Characterization of Met95 mutants of a heme-regulated phosphodiesterase from Escherichia coli. Optical absorption, magnetic circular dichroism, circular dichroism, and redox potentials, Eur. J. Biochem. 270, 4771-4779.
29. Mathews, F. S. (2001) in Handbook of Metalloproteins (Messerschmidt, A., Huber, R., Poulos, T., and Wieghardt, K., Eds.) Vol. 1, pp 159-171, John Wiley & Sons, Chichester.
30. Rotenberg, M., and Margalit, R. (1985) Deuteroporphyrin-albumin binding equilibrium. The effects of porphyrin self-aggregation studied for the human and the bovine proteins, Biochem. J. 229, 197-203.
31. Sato, A., Sasakura, Y., Sugiyama, S., Sagami, I., Shimizu, T., Mizutani, Y., and Kitagawa, T. (2002) Stationary and time-resolved resonance Raman spectra of His77 and Met95 mutants of the isolated heme domain of a direct oxygen sensor from Escherichia coli, J. Biol. Chem. 277, 32650-32658.
32. Vogel, K. M., Spiro, T. G., Shelver, D., Thorsteinsson, M. V., and Roberts, G. P. (1999) Resonance Raman evidence for a novel charge relay activation mechanism of the CO-dependent heme protein transcription factor CooA, Biochemistry 38, 2679-2687.
33. Hu, S. Z., Morris, I. K., Singh, J. P., Smith, K. M., and Spiro, T. G. (1993) Complete assignment of cytochrome c resonance Raman spectra via enzymic reconstitution with isotopically labeled hemes, J. Am. Chem. Soc. 115, 12446-12458.
34. Hu, S. Z., Smith, K. M., and Spiro, T. G. (1996) Assignment of protoheme resonance Raman spectrum by heme labeling in myoglobin, J. Am. Chem. Soc. 118, 12638-12646.
35. Uchida, T., Ishikawa, H., Takahashi, S., Ishimori, K., Morishima, I., Ohkubo, K., Nakajima, H., and Aono, S. (1998) Heme environmental structure of CooA is modulated by the target DNA binding. Evidence from resonance Raman spectroscopy and CO rebinding kinetics, J. Biol. Chem. 273, 19988-19992.
36. Takahashi, S., Wang, J., Rousseau, D. L., Ishikawa, K., Yoshida, T., Takeuchi, N., and Ikeda-Saito, M. (1994) Heme-heme oxygenase complex: structure and properties of the catalytic site from resonance Raman scattering, Biochemistry 33, 5531-5538.
37. Tamura, K., Nakamura, H., Tanaka, Y., Oue, S., Tsukamoto, K., Nomura, M., Tsuchiya, T., Adachi, S., Takahashi, S., Iizuka, T., and Shiro, Y. (1996) Nature of endogenous ligand binding to heme iron in oxygen sensor FixL, J. Am. Chem. Soc. 118, 9434-9435.
38. Rodgers, K. R., Lukat-Rodgers, G. S., and Barron, J. A. (1996) Structural basis for ligand discrimination and response initiation in the heme-based oxygen sensor FixL, Biochemistry 36, 9539-9548.
39. Lukat-Rodgers, G. S., and Rodgers, K. R. (1997) Characterization of ferrous FixL-nitric oxide adducts by resonance Raman spectroscopy, Biochemistry 36, 4178-4187.
40. Deinum, G., Stone, J. R., Babcock, G. T., and Marletta, M. A. (1996) Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy, Biochemistry 35, 1540-1547.
41. Kitagawa, T., Kyogoku, Y., Iizuka, T., and Ikeda-Saito, M. (1976) Nature of the iron-ligand bond in ferrous low spin hemoproteins studied by resonance Raman scattering, J. Am. Chem. Soc. 98, 5169-5173.
42. ∈ (His F8) stretching band in the resonance Raman spectra of deoxy myoglobin, FEBS Lett. 104, 376-378.
43. Kincaid, J., Stein, P., and Spiro, T. G. (1979) Absence of heme-localized strain in T state hemoglobin: insensitivity of heme-imidazole resonance Raman frequencies to quaternary structure, Proc. Natl. Acad. Sci. U.S.A. 76, 549-552.
44. Johnson, W. C. (1999) Analyzing protein circular dichroism spectra for accurate secondary structures, Proteins 35, 307-312.
45. Sreerama, N., and Woody, R. W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism, Anal. Biochem. 209, 32-44.
46. Sreerama, N., and Woody, R. W. (1994) Poly(pro)II helices in globular proteins: identification and circular dichroic analysis, Biochemistry 33, 10022-10025.
47. Muller-Eberhard, U., and Nikkila, H. (1989) Transport of tetrapyrroles by proteins, Semin. Hematol. 26, 86-104.
48. Iwahara, S., Satoh, H., Song, D. X., Webb, J., Burlingame, A. L., Nagae, Y., and Muller-Eberhard, U. (1995) Purification, characterization, and cloning of a heme-binding protein (23 kDa) in rat liver cytosol, Biochemistry 34, 13398-13406.
49. Beaven, G. H., Chen, S. H., D'Albis, A., and Gratzer, W. B. (1974) A spectroscopic study of the haemin-human-serum-albumin system, Eur. J. Biochem. 41, 539-546.
50. Blackmon, B. J., Dailey, T. A., Lianchun, X., and Dailey, H. A. (2002) Characterization of a human and mouse tetrapyrrole-binding protein, Arch. Biochem. Biophys. 407, 196-201.
51. Ignarro, L. J., Ballot, B., and Wood, K. S. (1984) Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins, J. Biol. Chem. 259, 6201-6207.
52. Ogawa, K., Sun, J., Taketani, S., Nakajima, O., Nishitani, C., Sassa, S., Hayashi, N., Yamamoto, M., Shibahara, S., Fujita, H., and Igarashi, K. (2001) Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1, EMBO J. 20, 2835-2843.
53. Horio, Y., and Murad, F. (1991) Solubilization of guanylyl cyclase from bovine rod outer segments and effects of lowering Ca2+ and nitro compounds, J. Biol. Chem. 266, 3411-3415.
54. Kutty, R. K., Kutty, G., Wiggert, B., Chader, G. J., Darrow, R. M., and Organisciak, D. T. (1995) Induction of heme oxygenase 1 in the retina by intense visible light: suppression by the antioxidant dimethylthiourea, Proc. Natl. Acad. Sci. U.S.A. 92, 1177-1181.
55. Schwartzman, M. L., Masferrer, J., Dunn, M. W., McGiff, J. C., and Abraham, N. G. (1987) Cytochrome P450, drug metabolizing enzymes and arachidonic acid metabolism in bovine ocular tissues, Curr. Eye Res. 6, 623-630.